Stress-activated MAPK signalling controls fission yeast actomyosin ring integrity by modulating formin For3 levels

  1. Elisa Gómez-Gil
  2. Rebeca Martín-García
  3. Jero Vicente-Soler
  4. Alejandro Franco
  5. Beatriz Vázquez-Marín
  6. Francisco Prieto-Ruiz
  7. Teresa Soto
  8. Pilar Pérez
  9. Marisa Madrid  Is a corresponding author
  10. Jose Cansado  Is a corresponding author
  1. Universidad de Murcia, Spain
  2. Instituto de Biología Funcional y Genómica/Universidad de Salamanca, Spain

Abstract

Cytokinesis, which enables the physical separation of daughter cells once mitosis has been completed, is executed in fungal and animal cells by a contractile actin- and myosin-based ring (CAR). In the fission yeast Schizosaccharomyces pombe the formin For3 nucleates actin cables and also co-operates for CAR assembly during cytokinesis. Mitogen-Activated Protein Kinases (MAPKs) regulate essential adaptive responses in eukaryotic organisms to environmental changes. We show that the Stress Activated Protein Kinase pathway (SAPK) and its effector, MAPK Sty1, downregulates CAR assembly in S. pombe when its integrity becomes compromised during cytoskeletal damage and stress by reducing For3 levels. Accurate control of For3 levels by the SAPK pathway may thus represent a novel regulatory mechanism of cytokinesis outcome in response to environmental cues. Conversely, SAPK signalling favours CAR assembly and integrity in its close relative S. japonicus, revealing a remarkable evolutionary divergence of this response within the fission yeast clade.

Data availability

All data generated or analysed during this study are included within the manuscript and supporting files.

Article and author information

Author details

  1. Elisa Gómez-Gil

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. Rebeca Martín-García

    Morfogénesis y Polaridad Celular, Instituto de Biología Funcional y Genómica/Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Jero Vicente-Soler

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Alejandro Franco

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Beatriz Vázquez-Marín

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Francisco Prieto-Ruiz

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Teresa Soto

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2965-318X
  8. Pilar Pérez

    Morfogénesis y Polaridad Celular, Instituto de Biología Funcional y Genómica/Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.
  9. Marisa Madrid

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    For correspondence
    marisa@um.es
    Competing interests
    The authors declare that no competing interests exist.
  10. Jose Cansado

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    For correspondence
    jcansado@um.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2342-8152

Funding

Ministerio de Economía y Competitividad (BFU2017-82423-P)

  • Jose Cansado

Ministerio de Economía y Competitividad (PGC2018-098924-B-100)

  • Pilar Pérez

Junta de Castilla y Leon (CLU-2017-03)

  • Pilar Pérez

Fundacion Seneca (20856/PI/18)

  • Jose Cansado

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2020, Gómez-Gil et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,841
    views
  • 279
    downloads
  • 17
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Elisa Gómez-Gil
  2. Rebeca Martín-García
  3. Jero Vicente-Soler
  4. Alejandro Franco
  5. Beatriz Vázquez-Marín
  6. Francisco Prieto-Ruiz
  7. Teresa Soto
  8. Pilar Pérez
  9. Marisa Madrid
  10. Jose Cansado
(2020)
Stress-activated MAPK signalling controls fission yeast actomyosin ring integrity by modulating formin For3 levels
eLife 9:e57951.
https://doi.org/10.7554/eLife.57951

Share this article

https://doi.org/10.7554/eLife.57951

Further reading

    1. Cell Biology
    2. Neuroscience
    Naoki Yamawaki, Hande Login ... Asami Tanimura
    Research Article

    The claustrum complex is viewed as fundamental for higher-order cognition; however, the circuit organization and function of its neuroanatomical subregions are not well understood. We demonstrated that some of the key roles of the CLA complex can be attributed to the connectivity and function of a small group of neurons in its ventral subregion, the endopiriform (EN). We identified a subpopulation of EN neurons by their projection to the ventral CA1 (ENvCA1-proj. neurons), embedded in recurrent circuits with other EN neurons and the piriform cortex. Although the ENvCA1-proj. neuron activity was biased toward novelty across stimulus categories, their chemogenetic inhibition selectively disrupted the memory-guided but not innate responses of mice to novelty. Based on our functional connectivity analysis, we suggest that ENvCA1-proj. neurons serve as an essential node for recognition memory through recurrent circuits mediating sustained attention to novelty, and through feed-forward inhibition of distal vCA1 neurons shifting memory-guided behavior from familiarity to novelty.

    1. Cell Biology
    2. Computational and Systems Biology
    Sarah De Beuckeleer, Tim Van De Looverbosch ... Winnok H De Vos
    Research Article

    Induced pluripotent stem cell (iPSC) technology is revolutionizing cell biology. However, the variability between individual iPSC lines and the lack of efficient technology to comprehensively characterize iPSC-derived cell types hinder its adoption in routine preclinical screening settings. To facilitate the validation of iPSC-derived cell culture composition, we have implemented an imaging assay based on cell painting and convolutional neural networks to recognize cell types in dense and mixed cultures with high fidelity. We have benchmarked our approach using pure and mixed cultures of neuroblastoma and astrocytoma cell lines and attained a classification accuracy above 96%. Through iterative data erosion, we found that inputs containing the nuclear region of interest and its close environment, allow achieving equally high classification accuracy as inputs containing the whole cell for semi-confluent cultures and preserved prediction accuracy even in very dense cultures. We then applied this regionally restricted cell profiling approach to evaluate the differentiation status of iPSC-derived neural cultures, by determining the ratio of postmitotic neurons and neural progenitors. We found that the cell-based prediction significantly outperformed an approach in which the population-level time in culture was used as a classification criterion (96% vs 86%, respectively). In mixed iPSC-derived neuronal cultures, microglia could be unequivocally discriminated from neurons, regardless of their reactivity state, and a tiered strategy allowed for further distinguishing activated from non-activated cell states, albeit with lower accuracy. Thus, morphological single-cell profiling provides a means to quantify cell composition in complex mixed neural cultures and holds promise for use in the quality control of iPSC-derived cell culture models.